Continental-scale patterns of Cecropia reproductive phenology: evidence from herbarium specimens.

Abstract

Plant phenology is concerned with the timing of recurring biological events. Though phenology has traditionally been studied using intensive surveys of a local flora, results from such surveys are difficult to generalize to broader spatial scales. In this study, contrastingly, we assembled a continental-scale dataset of herbarium specimens for the emblematic genus of Neotropical pioneer trees, Cecropia, and applied Fourier spectral and cospectral analyses to investigate the reproductive phenology of 35 species. We detected significant annual, sub-annual and continuous patterns, and discuss the variation in patterns within and among climatic regions. Although previous studies have suggested that pioneer species generally produce flowers continually throughout the year, we found that at least one third of Cecropia species are characterized by clear annual flowering behaviour. We further investigated the relationships between phenology and climate seasonality, showing strong associations between phenology and seasonal variations in precipitation and temperature. We also verified our results against field survey data gathered from the literature. Our findings indicate that herbarium material is a reliable resource for use in the investigation of large-scale patterns in plant phenology, offering a promising complement to local intensive field studies.

Full text

Page 1

doi: 10.1098/rspb.2010.2259
published online 12 January 2011
Proc. R. Soc. B
Sarmiento, Daniel Sabatier and Patrick Heuret
Paul-Camilo Zalamea, François Munoz, Pablo R. Stevenson, C. E. Timothy Paine, Carolina
phenology: evidence from herbarium specimens
reproductive
Cecropia
Continental-scale patterns of


Supplementary data
tml
http://rspb.royalsocietypublishing.org/content/suppl/2011/01/07/rspb.2010.2259.DC1.h
"Data Supplement"
References
ml#ref-list-1
http://rspb.royalsocietypublishing.org/content/early/2011/01/07/rspb.2010.2259.full.ht

This article cites 27 articles, 1 of which can be accessed free
P<P
Subject collections
Published online 12 January 2011 in advance of the print journal.
(478 articles)environmental science
?
(2074 articles)ecology
?

Articles on similar topics can be found in the following collections
Email alerting service

here
right-hand corner of the article or click
Receive free email alerts when new articles cite this article - sign up in the box at the top
publication.
Citations to Advance online articles must include the digital object identifier (DOIs) and date of initial
online articles are citable and establish publication priority; they are indexed by PubMed from initial publication.
the paper journal (edited, typeset versions may be posted when available prior to final publication). Advance
Advance online articles have been peer reviewed and accepted for publication but have not yet appeared in

http://rspb.royalsocietypublishing.org/subscriptions
go to: Proc. R. Soc. BTo subscribe to
This journal is © 2011 The Royal Society
on January 12, 2011 rspb.royalsocietypublishing.orgDownloaded from

Page 2

Continental-scale patterns of Cecropia
reproductive phenology: evidence from
herbarium specimens
Paul-Camilo Zalamea1,2,*,†, Franc ¸ois Munoz3, Pablo R. Stevenson2,
C. E. Timothy Paine4, Carolina Sarmiento2, Daniel Sabatier1
and Patrick Heuret5,*
1IRD, UMR AMAP , Montpellier 34000, France
2Departamento de Ciencias Biolo ´gicas, Universidad de Los Andes, Bogota ´, Colombia
3Universite ´ Montpellier 2, UMR AMAP , Montpellier 34000, France
4Institut fu ¨r Evolutionsbiologie und Umweltwissenschaften, Universita ¨t Zu ¨rich, Zu ¨rich, Switzerland
5INRA, UMR Ecologie des Fore ˆts de Guyane, Kourou 709-97387, French Guiana
Plant phenology is concerned with the timing of recurring biological events. Though phenology has
traditionally been studied using intensive surveys of a local flora, results from such surveys are difficult
to generalize to broader spatial scales. In this study, contrastingly, we assembled a continental-scale data-
set of herbarium specimens for the emblematic genus of Neotropical pioneer trees, Cecropia, and applied
Fourier spectral and cospectral analyses to investigate the reproductive phenology of 35 species. We
detected significant annual, sub-annual and continuous patterns, and discuss the variation in patterns
within and among climatic regions. Although previous studies have suggested that pioneer species gener-
ally produce flowers continually throughout the year, we found that at least one third of Cecropia species
are characterized by clear annual flowering behaviour. We further investigated the relationships between
phenology and climate seasonality, showing strong associations between phenology and seasonal vari-
ations in precipitation and temperature. We also verified our results against field survey data gathered
from the literature. Our findings indicate that herbarium material is a reliable resource for use in the
investigation of large-scale patterns in plant phenology, offering a promising complement to local
intensive field studies.
Keywords: climate seasonality; reproductive patterns; Fourier spectral and cospectral analyses;
herbarium collections; Neotropics; pioneer plants
1. INTRODUCTION
Plant phenology can be defined as the study of the timing
of recurring biological events, its causes with regard to
biotic and abiotic forces, and the relation among phases
of the same or different species [1]. The most common
method to assess plant phenology is to survey local popu-
lations repeatedly over many years [2–5]. Correlative
approaches have frequently shown phenological par-
ameters to change in concert with environmental
variables. Variation in precipitation, soil water availability,
temperature, irradiance and day length seem to control
the periodicity of flowering and leaf abscission in many
tropical species [3–7]. Understanding the links between
phenological patterns and environmental variables is cru-
cial to advance the study of community and species
dynamics under various climate change scenarios. By
studying phenology at the continental scale, over which
climate varies, we may improve our understanding of
species dynamics and their interactions with climate. In
this contribution, we use herbarium collections as a
data source, because they can provide valuable infor-
mation on species distribution and description of
reproductive patterns at large geographical scales [8,9].
The periodicity of phenological events can be classified
as continuous, sub-annual, annual or supra-annual [10].
However, there is no consensus on the appropriate stat-
istical method to characterize these patterns. Circular
statistics are frequently used to analyse phenology,
though these methods fail to describe sub-annual and
supra-annual patterns [5]. In contrast, Fourier spectral
analysis allows for a more general investigation of periodic
patterns in spatial and temporal contexts [11–13].
Although Fourier spectral analysis has been used to
study periodic patterns in many datasets (e.g. [14]), it
has not yet been used to explore phenological patterns.
The Neotropical genus Cecropia Loefl. (Urticaceae)
includes 61 species distributed across a wide range of
climates from southern Mexico to northern Argentina
[15]. With some very widespread species, Cecropia is an
emblematic genus of pioneer trees in the Neotropics
[15]. Published observations on Cecropia phenology are
scarce. Zalamea et al. [16] found flowering to be strongly
annual in C. sciadophylla in Colombia and French
* Authors for correspondence (camilozalamea@gmail.com; patrick.
heuret@ecofog.gf).
†Present address: Instituto de Investigacio ´n de Recursos Biolo ´gicos
Alexander von Humboldt, Bogota ´, Colombia.
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rspb.2010.2259 or via http://rspb.royalsocietypublishing.org.
Proc. R. Soc. B
doi:10.1098/rspb.2010.2259
Published online
Received 18 October 2010
Accepted 13 December 2010
1
This journal is q 2011 The Royal Society
on January 12, 2011 rspb.royalsocietypublishing.orgDownloaded from

Page 3

Guiana, though, in their systematic monograph of the
genus, Berg & Franco [15] indicate that most Cecropia,
including C. sciadophylla, produce flowers and fruits
throughouttheyear. These apparently contradictory results
may arise from variation in phenology among regions, illus-
trating the importance of studying phenology at large
geographical scales.
In this study, we examined the temporal patterns in
Cecropia reproductive phenology throughout the Neotro-
pics using Fourier spectral analyses. Following the
hypothesis that climate seasonality is a primary driver of
Cecropia phenology, we defined geographical regions
comprisingsimilar bioclimatic
assessed the strength of climatic determinants on Cecropia
phenology. Furthermore, we tested whether the periodic
structures are related to rainfall and temperature season-
ality using cospectral analysis and non-parametric tests.
Finally, we surveyed the available literature on Cecropia
phenology to determine the consistency of patterns
inferred from herbarium specimens and field surveys.
conditions, andwe
2. MATERIAL AND METHODS
(a) Assignment of bioclimatic regions
We investigated whether climate seasonality could drive
Cecropia phenology and generate within-species, as well as
among-species, variation. We gathered interpolated monthly
averages of precipitation, and minimum and maximum temp-
eratures from 1950 to 2000 (WorldClim dataset, http://
worldclim.org [17]). We then divided the study area (i.e. ter-
restrial portion of the area between 248N, 1048W and 318
S, 348W) into 20 by 20 km pixels (i.e. 44385 pixels in
total) and averaged the bioclimatic values within each pixel.
We performed a principal component analysis (PCA) of
these pixel data and performed a k-means classification of
the resulting scores to get bioclimatic regions (figure 1). We
classified the pixels into nine regions because this is the
finest scale at which we could analyse the available data, and
these regions were largely congruent with more classical,
descriptive classifications (see [18]). The nine bioclimatic
regions were characterized by (i) low precipitation and low
temperature (Andes and Central America mountains), (ii) a
dry season in the first half of the year and low annual precipi-
tation (dry Central America and Caribbean), (iii) a dry season
in the first half of the year and high annual precipitation (Ori-
noquı ´a and humid Central America), (iv) no seasons and very
high annual precipitation (West Amazonia and Choco), (v) a
dry season in the middle of the year and high annual precipi-
tation (South Amazonia), (vi) a dry season in the second half
of the year (Guiana Shield), (vii) a dry season in the middle of
the year and low variation in temperature (Caatinga and Cer-
rado), (viii) a dry season in the middle of the year, high
variation in temperature and predominance of dry months
(West Austral zone), and (ix) a dry season in the middle of
the year, high variation in temperature and predominance of
humid months (East Austral zone).
(b) Herbarium dataset
We examined Cecropia collections at New York Botanical
Garden Herbarium (NY, n ¼ 880), Colombian National
Herbarium(COL,
n ¼ 697),
Museum Herbarium (P, n ¼ 142), Colombian Amazon
Herbarium (COAH, n ¼ 117), French Guiana Herbarium
(CAY, n ¼ 82), University of Panama Herbarium (PMA,
Paris NaturalHistory
n ¼ 58) and Suriname National Herbarium (BBS, n ¼ 19).
We gathered information on collection date, species, locality
and sex for a total of 1995 fertile specimens representing all
61 species described for the genus [15]. We further obtained
similar information from the herbarium data presented in
Flora Neotropica [15], expanding our dataset to a total of
3668 fertile specimens for the 61 Cecropia species. We were
careful to not include the same voucher information more
than once. We then attributed species and bioclimatic
region labels to the herbarium specimens, and established
70 species–region combinations that included at least 15
herbarium specimens. Thirty-five different Cecropia species
and a total of 3382 fertile specimens were represented in
this subset of 70 species–regions. Given that several species
of Cecropia have a low number of collections, we used
the15-herbarium specimens threshold as criterion to ensure
that we had enough sampled species–regions for subsequent
statistical analyses (for more detail in the number of speci-
mens needed to detect periodicity in phenology, see
appendix S1 in electronic supplementary material).
In herbarium samples of Cecropia, fruits are not easily dis-
tinguishable from female flowers, whereas the flowering stage
is unambiguous for male individuals. As a preliminary analy-
sis, we used a linear mixed effects model to check for any
differences between the number of male and female collec-
tions among months. We coded collections as response
variable, sex and month as fixed effects, and species as
random effect, with the number of collections per month
modelled as a Poisson distribution. We found no significant
difference between the number of male and female collec-
tions among months (n ¼ 1352 and 2030, respectively;
d.f. ¼ 1, t ¼ 6.021, p ¼ 0.105). Thus, we grouped male and
female specimens and refer to them all as ‘flowering’samples.
(c) Fourier spectral and cospectral analyses
We applied Fourier analysis to detect periodicity in the
herbarium phenology data. Fourier spectral analysis decom-
poses a time series into a sum of sinusoidal components
representing periodic trends of varying periods [19]. The
analysis could detect six periodic components (i.e. 12, 6, 4,
3, 2.4 and 2 months); longer and shorter components were
not detectable from the twelve-month sampling (see [20]
and appendix S2 in electronic supplementary material).
The normalized amplitudes of the components correspond
to the percentage of variation they each explain and,
altogether, comprise the Fourier spectrum. Thus, a periodic
component of amplitude 0.5 explains 50 per cent of the over-
all variation of the time series. Phenological patterns were
declared significant if the amplitude of at least one of their
periodic components surpassed the 95 per cent limits of a
null model with no periodic structure, which we obtained
by randomly permuting the monthly data 10 000 times.
We applied this methodological framework for the
species–region data, and we restricted subsequent analyses
to the spectra displaying at least one significant component.
We performed a PCA of the significant spectra, and a
2-means classification (k-means function) of their scores to
test a potential dichotomy in periodic patterns for the
Cecropia species. Thus, we sought to distinguish annual
patterns from all sub-annual patterns, which include
periodicities of more than one cycle per year.
We assessed whether periodic variation in phenology was
related to a periodic pattern in climate variation using
Fourier cospectral analyses. In these analyses, the relative
2P.-C. Zalamea et al.
Cecropia phenology at continental scale
Proc. R. Soc. B
on January 12, 2011 rspb.royalsocietypublishing.orgDownloaded from

Page 4

amplitudes of the periodic components helped to check the
covariation of periodic trends [19]. We performed, analo-
gously with the spectral analysis, 10 000 randomizations of
the monthly data to determine significant periodic trends of
covariation inphenological
interpolated monthly averages of precipitation and median
temperatures [17]). Any component that surpassed the 95
per cent null distribution indicated a significant association
between the periodic phenological pattern and climatic
variable. For any significant annual structure, we further
andclimatic data (i.e.
measured the time lag between the climatic parameter peak
and the species flowering response using the corresponding
phase within the Fourier cospectral analysis. Thus, when
the reproductive phenology and climate variables follow an
annual behaviour, an observed six-month lag refers to a
reproductive peak coinciding with the minima of the climatic
variable.
All analyses were performed using the R software and
multivariate analyses were performed using the ade4 package
[21,22].
month monthmonth
0
100
200
300
0
10
20
30
precipitation (mm)
temperature (°C)
0
10
20
30
temperature (°C)
0
10
20
30
temperature (°C)
0
100
200
300
precipitation (mm)
0
100
200
300
–30° S
–20° S
–10° S
0°
10° N
20° N
100° W 90° W80° W70° W60° W50° W40° W
S
E
N
W
precipitation (mm)
JMMJSNJMMJSNJMMJSN
(vii) Caatinga and Cerrado
ap = 1043 mm
(ix) East Austral zone
ap = 1581 mm
(viii) West Austral zone
ap = 851 mm
(i) Andes and Central America
mountains
ap = 538 mm
(iv) West Amazonia and Choco
ap = 3005 mm
(v) South Amazonia
ap = 1319 mm
(vi) Guiana Shield
ap = 2184 mm
(ii) dry Central America and
Caribbean
ap = 1319 mm
(iii) Orinoquía and humid Central
America
ap = 2593 mm
Figure 1. Nine climatic regions map delimited by a 9-means cluster analysis. The circles in the map symbolize the positions of
the studied Cecropia herbarium specimens. In addition, for each region mean annual precipitation (bars), maximum (grey line)
and minimum (black line) temperatures are showed. For all panels ap is the average annual precipitation in millimetres.
Cecropia phenology at continental scale
P.-C. Zalamea et al.
3
Proc. R. Soc. B
on January 12, 2011rspb.royalsocietypublishing.orgDownloaded from

Page 5

(d) Consistency with field-survey information
We surveyed the literature on Cecropia phenology to deter-
mine the extent to which flowering peaks and frequencies
inferred from herbarium specimens are consistent with the
published literature based on field surveys. Data gathering
included our prior knowledge of the literature, and searches
in Web of Science (http://www.isiwebofknowledge.com) and
Google Scholar (http://scholar.google.com) using the key
words ‘Cecropia’ and ‘phenology’.
3. RESULTS
(a) Flowering frequencies in climatic regions
The flowering phenology of 25 of the 70 species–region
combinations displayed significant periodicity (randomiz-
ation test, p , 0.05). The 2-means classification of the
significant spectra distinguished 18 species–regions with
a prominent first component (i.e. annual flowering pat-
tern;figure2a
andthe
material, table S1) and seven species–regions with stron-
ger secondary components (i.e. sub-annual flowering
patterns; figure 2b). The remaining 45 species–region
electronicsupplementary
combinations did not display any significant periodicity
(p ? 0.05). This group included species with continuous
flowering, species that flower irregularly and species with
undetected patterns of periodic variation (see electronic
supplementary material, appendix S1).
(b) Association of climate and phenology in
annual species
Fouriercospectra of precipitationandphenologyweresigni-
ficant for all the 18 species–region combinations displaying
annual patterns, as well as for all cospectra of median temp-
erature and phenology (randomization test, p , 0.05). This
indicatedthattheannualpatternsofphenologywerestrongly
associated with annual patterns in climate. On the other
hand, the phase of the cospectra, which represents the
lag between the climatic and the flowering peaks, broa-
dly varied between temperature- and precipitation-based
cospectra (see electronic supplementary material, table S1).
We illustrate these results using observations from two
species–regions: C. sciadophylla in the Guiana Shield
region, and
C. mutisiana
(figure 3). For C. sciadophylla, the amplitude of the
annual component of the precipitation and temperature
cospectra exceeded that expected by chance, indicating
asignificantlinkbetween
(figure 3e,g). For C. mutisiana, the precipitation cospec-
trumshowed asignificant
generated by the combination of annual variation in
phenology and a bi-annual variation in precipitation
(figure 3f ). The temperature cospectrum, on the other
hand, contained a significant annual component, as
there is a single annual peak in temperature, suggesting
that the annual flowering of this species could be more
closely linked with temperature than with precipitation.
The number of annual flowering species in each bio-
climatic region was not evenly distributed across the
Neotropics; we found regions with zero, one or more
annual flowering species. Table S1 in the electronic sup-
plementary material shows that the timing of peak
flowering varied within regions, among species and
among regions. The flowering peaks of species were tem-
porally synchronous in some regions, such as the Guiana
Shield. Cecropia obtusa, C. palmata and C. sciadophylla
flower during September–October, which corresponds to a
six month lag with the precipitation peak, and at the time
when temperatures are greatest (see electronic supplemen-
tary material, table S1). On the contrary, other species
within regions are desynchronized. For example, in the dry
Central America and Caribbean region, C. peltata flowered
in July, close to the precipitation and temperature peaks,
whereas C.obtusifolia and C. schreberianaflowered inMarch.
inthe Andesregion
phenologyandclimate
six-monthcomponent,
(c) Consistency with field-survey information
Although available observations on Cecropia phenology
are scarce, some authors include Cecropia species among
extensive lists of phenological information ([5]; for a
detailed references list see appendix S3 in the electronic
supplementary material). Table 1 provides a summary
of Cecropia phenology data from the present study and
from the field survey data gathered from the literature.
We found that herbarium flowering peaks for annual
species are within one month of the flowering peaks docu-
mented in the literature (table 1). However, flowering
Fourier component
(a)
amplitude
(b)
1 (12 mo)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
amplitude
0
0.2
0.4
0.6
0.8
2 (6 mo) 3 (4 mo) 4 (3 mo) 5 (2.4 mo) 6 (2 mo)
Figure 2. Box-plotsrepresentingtherelativeimportanceofper-
iodiccomponentsinFourierspectraforspecies–regions(a)with
significant annual patterns in flowering (first box-plot on the
left) and (b) with significant sub-annual patterns. The number
of months between brackets represents the corresponding
period, and the bold bar represents the median.
4P.-C. Zalamea et al.
Cecropia phenology at continental scale
Proc. R. Soc. B
on January 12, 2011rspb.royalsocietypublishing.orgDownloaded from

Page 6

periods inferred from herbaria are on average two
months longer than those inferred from field surveys.
Furthermore, the literature suggests that C. membranacea,
C. hololeuca, C. glasiovii, C. angustifolia and C. reticulata
flower continuously throughout the year. Our results are
consistent with these findings, as those species showed no
significant periodic structure in our analysis (table 1).
In general, our data from herbarium specimens agree
with field survey data, with one exception: our analysis
detected no periodic pattern for C. latiloba, which is
reported to have annual periodicity (table 1 [23]).
4. DISCUSSION
(a) Cecropia flowering frequencies
We found that 18 Cecropia species (representing 29.5 per
cent of species in the genus) and 41 per cent of the
studied species flower annually. This result contrasts
with the traditional view that pioneer plants in tropical
forests flower copiously and continuously once they
attain maturity [24]. In contrast, 13 dominant pioneer
species near Manaus, Brazil have been shown to flower
annually [25]. Our results reinforce and generalize the
finding of annual reproductive phenology for an emble-
matic genus of pioneer trees across the Neotropics.
In our survey, the group of species lacking periodic
structure included some Cecropia species that were pre-
viously reported as continuously flowering (table 1),
which is consistent with our results. However, some of
the species for which we did not detect periodic structure
may actually have significant flowering patterns. These
patterns may be undetectable because their flowering
periods or the time until fruit maturity are so lengthy
that fertile specimens can be collected year-round.
Another factor that may obscure periodic structure is
the number of specimens used in the analysis. We evalu-
ated the relationship between sample size and the power
to detect phenological patterns with a simulation, which
indicated that the type II (false negative) error rate
decreases with sample size. Given simulated data with
an annual pattern, there is a 70 per cent probability of
failing to detect the pattern with a sample size of 15 her-
barium specimens, but this probability drops to 5 per cent
with a sample size of 60 specimens (see the electronic
supplementary material, appendix S1). On the other
hand, the type I (false positive) error rate is approximately
12 mo
Jan FebMarAprMay Jun Jul
month
AugSep Oct NovDec Jan FebMarAprMay Jun Jul
month
AugSep Oct NovDec
0
temperature
cospectrum
precipitation
cospectrum
0
100
200
300
0
50
100
150
200
250
(a)
precipitation (mm)
(b)
250
(c)
collection frequency
(d)
0.30
(e)
(f)
(g)(h)
0
median temperature
variation (°C)
50
100
150
200
0
0.15
0.30
0
0
20
40
60
80
0.15
0
0.4
0.8
1.2
0
0.4
0.8
1.2
0.5
1.0
1.5
0
0.2
0.4
0.6
6 mo4 mo3 mo
period
2.4 mo2 mo12 mo6 mo4 mo
period
3 mo2.4 mo2 mo
Figure 3. Monthly averages of precipitation (bars) and median temperature variation (lines) for (a) C. sciadophylla and
(b) C. mutisiana collections. Median temperature variation is calculated as (tmonth2tmin)/2, where tmonthis the temperature
of each month and tminis the minimum temperature. Frequency of fertile herbarium collections by month of (c) C. sciadophylla
from the Guiana Shield region (n ¼ 40; climatic region vi) and (d) C. mutisiana from the Andes region (n ¼ 25; climatic region
i). Fourier cospectra of phenology and precipitation (bars), and the 97.5% confidence limit of the null model for the Fourier
cospectra (lines) for (e) C. sciadophylla and (f ) C. mutisiana, as well as Fourier cospectra of phenology and median temperature
(bars), and the 97.5% confidence limit of the null model for the Fourier cospectra (lines) for (g) C. sciadophylla and
(h) C. mutisiana.
Cecropia phenology at continental scale
P.-C. Zalamea et al.
5
Proc. R. Soc. B
on January 12, 2011rspb.royalsocietypublishing.org Downloaded from

Page 7

Table 1. Summary of Cecropia phenology data based on herbarium specimens and literature sources. Species are presented following the region classification used to analyse the data.
flowering (herbarium)
flowering (literature)
region
species
period
peak
frequency
period
peak
frequency
site
referencea
Andes and Central America mountains (climatic region i)
C. mutisianab
Dec–Jul
Mar
annual
C. obtusifoliab
Dec–Jun
Mar
annual
C. strigosab
Oct–Apr
Dec
annual
C. reticulatad
Jan–Dec
non-annual
continuous
Alto Yunda, Colombia
[1]
C. angustifoliad
Jan–Dec
non-annual
Jan–Dec
continuous
Cotapata, Bolivia
[2]
dry Central America and Caribbean (climatic region ii)
C. obtusifoliab
Dec–Aug
Apr
annual
Feb–Sep
Apr
annual
BCI, Panama
[3]
C. peltatab
Apr–Nov
Jul
annual
Feb–Oct
Jun
annual
Santa Rosa Guanacaste, Costa Rica
[4,5]
C. schreberianab
Jan–Sep
Apr
annual
Nov–Jun
Apr
annual
Luquillo Monuntains, Puerto Rico
[6,7]
C. longipesc
May–Nov
Aug
annual
Panama City, Panama
[8]
C. insignisc
Jan–Jul
Feb
annual
BCI, Panama
[3,6]
C. heterochromab
Jan–Apr/Jul-Sep
Mar/Aug
bi-annual
humid Central America and Orinoquı ´a (climatic region iii)
C. obtusifoliad
Jan–Dec
non-annual
Jan–Dec
continuous
La Selva, Costa Rica
[9]
C. insignisb
Sep–Mar
Mar
annual
Feb–Jul
Apr
annual
La Selva, Costa Rica
[9,10]
C. peltatab
Mar–Oct
Jun
annual
C. sciadophyllad
Sep–Mar
non-annual
Oct–Mar
Jan
annual
Tinigua NP, Colombia
[11]
C. membranacead
Jun–Apr
non-annual
Jan–Sep
continuous
Tinigua NP, Colombia
[12,13]
West Amazonia (climatic region iv)
C. distachyab
Jun–Jan
Oct
annual
South Amazonia (climatic region v)
C. englerianab
Feb–Aug
May
annual
C. utcubambanab
Jun–Dec
Aug
annual
C. concolorb
Aug–Feb
Nov
annual
Nov–Apr
Dec
annual
Santa Cruz, Bolivia
[14]
C. polystachyab
Aug–Feb
Nov
annual
C. purpurascensc
Jun–Dec
Sep
annual
BDFFP, Manaus, Brazil
[15]
C. sciadophyllad
Apr–Nov
non-annual
Aug–Feb
Oct
annual
BDFFP, Manaus, Brazil
[15]
C. latilobad
Jan–Dec
non-annual
Apr–Aug
May
annual
Marchantaria, Manaus, Brazil
[16–18]
Guiana Shield (climatic region vi)
C. obtusab
Jun–Nov
Sep
annual
Aug–Nov
Sep
annual
Paracou, French Guiana
[19]
C. palmatab
Aug–Jan
Oct
annual
Oct–Jan
Nov
annual
French Guiana
[20]
C. sciadophyllab
Jul–Jan
Oct
annual
Sep–Dec
Nov
annual
ARBOCEL, French Guiana
[11,20,21]
Caatinga and Cerrado (climatic region vii)
C. pachystachyab
Aug–Feb
Dec
annual
Oct–May
Jan
annual
mid-west Parana ´, Brazil
[22]
C. saxatilisb
Dec–Jun
Feb
annual
C. hololeucad
Jan–Dec
non-annual
Jan–Dec
continuous
Sa ˜o Paulo, Brazil
[23,24]
C. glazioviid
Jan–Dec
non-annual
Jan–Dec
continuous
Sa ˜o Paulo, Brazil
[24,25]
aFor a references list, see appendix S3 in the electronic supplementary material.
bSignificant species based on a randomization test of Fourier spectra (significance level set to 5%).
cAnnual flowering species reported in the literature but not analysed in this study due to the low number of entries per region.
dNon-significant species based on the randomization test of Fourier spectra.
6P.-C. Zalamea et al.
Cecropia phenology at continental scale
Proc. R. Soc. B
on January 12, 2011 rspb.royalsocietypublishing.org Downloaded from

Page 8

5 per cent, regardless of sample size. Thus, our analysis
may have failed to detect some annual patterns, especially
in species–region combinations with small sample sizes,
but is unlikely to mistakenly report annual patterns.
More than 75 per cent of the 70 species–regions used
in the analysis were represented by at least 20 specimens.
(b) Shifting patterns and association with climate
seasonality
For all annually flowering species, phenology was signifi-
cantly associated with annual patterns of precipitation
and mean temperature. This result supports the many
studies that have shown strong associations between flow-
ering, precipitation and temperature patterns [6,7,9].
Although our results indicate that climate seasonality is
associated with Cecropia phenology, determining the indi-
vidual roles of temperature and precipitation was not
possible in this observational study. Further investigations
will be necessary to clarify the specific conditions that
trigger flower set. Specifically, large-scale potential habitat
modelling [26] could assess the causal relationships
between phenology and climate by independently investi-
gating the spatial association of species presence/absence
and bioclimatic information.
In this study, we found great variation among regions in
the number of annually flowering species, which we attri-
bute to the differences in seasonality among regions.
West Amazonia is characterized by an aseasonal climate
and very high annual precipitation, whereas regions such
as theGuianaShieldand
characterized by distinct climate seasonality (figure 1).
Correspondingly, the frequency of annually flowering
species is greater in the Guiana Shield and South
Amazonia than in West Amazonia, lending additional
support to the conclusion that Cecropia annual repro-
ductive phenology is linked to climate seasonality.
Furthermore, when we analysed the phenology of species
over their entire distribution ranges without splitting
them into bioclimatic regions (results not shown), we
found a reduction in the total number of species character-
ized by an annual flowering pattern (i.e. 11 instead of 18
species), although the detection of periodic patterns is
improved when the numberof samples increased (see elec-
tronic supplementary material, appendix S1). This might
be due to the fact that the timing of flowering peaks may
vary among climatic regions, causing the phenological
structure to appear uniform at a continental scale.
An interesting case is C. sciadophylla, a species distrib-
uted throughout the Amazon basin, the Guiana Shield
and the Orinoquı ´a region of Colombia and Venezuela
[15]. This species appeared to lack periodic structure
when considered across its range, while it was clearly
annual in species–region analyses (table 1). This con-
clusion is consistent with other studies that found
annual periodicity in flower production in local popu-
lations, but with different flowering peaks throughout
the year in different regions ([16,25,27,28]; J. Dalling &
M. Rios 2009, personal communication.).
Non-climatic factorsmay
phenology. Cecropia latiloba is a highly flood-tolerant species
widely distributed throughout the Amazon basin, for which
Scho ¨ngart et al. [23] found a high annual flowering
periodicity in a population near Manaus. Data gathered
SouthAmazoniaare
alsoaffect
Cecropia
from herbarium specimens for South Amazonia, however,
suggest a non-annual pattern for this species (table 1).
The observation that flowering in C. latiloba is responsive
to the timing of flooding may provide an explanation
[23]. Variation in flooding duration and extent among
rivers and years may affect C. latiloba phenology. Similarly,
J. Dalling & M. Rios (personal communication, 2009)
found that the ‘pungara’ type of C. membranacea, which is
associated with terra firme forests, has a continuous
flowering pattern, whereas the ‘herrerensis’ type, associated
with floodplain forests, has an annual pattern at Los
Amigos Biological Station, Peru [15]. Together, these
observations suggest that moisture parameters other than
precipitation may affect the phenology of some Cecropia
species.
(c) Sampling context
Herbarium-derived datasets allow broad-based phenolo-
gical analysis, but may reflect collecting biases. One of
the most important issues regarding herbarium data is
that collection dates of voucher specimens could be
non-randomly distributed throughout the year, due to
collector preferences. Boulter et al. [9] still showed that
the total number of specimens collected in a month was
randomly distributed across the course of the year for
the Queensland Herbarium (BRI). Additionally, for the
French Guiana Herbarium (CAY) we found that the
total number of collections per month was randomly
distributed throughout the year (runs test; n ¼ 109 295,
p ¼ 0.5). Thus, we do not believe our results to be
biased by temporal patterns in botanical collecting.
Phenological field studies are, normally, detailed obser-
vations in a limited area, whereas herbarium collections
cover a large spatial extent and allow a broad view of the
variation in phenology throughout the range of a species
[8,9]. However, inferences from herbarium-based studies
could be biased by the geographical distribution of botani-
cal collecting. In the Neotropics, botanical collections
are often concentrated near cities and research stations
[29]. For this study, we had relatively few specimens from
the Amazonia and Orinoquı ´a regions, limiting our scope
for inference in these areas.
There is a declining trend in the collection of herbar-
ium specimens, despite the utility of these collections in
systematic, biogeographic, plant invasion and applied
ecology studies [30]. The limited number of herbarium
specimens available for some Cecropia species precluded
analyses of their phenology. Our results show that herbar-
ium reproductive phenologies are consistent with field
studies and do not require as much time as field
monitoring, but sample size of herbarium specimens is
an important limit to their use.
(d) Fourier analysis in phenological studies
Most current methodologies to study phenological pat-
terns fail to describe some phenological behaviours. For
instance, recent studies in phenology have used circular
statistics [2,5,31,32], but such techniques give unsatisfac-
tory results for sub-annual and supra-annual patterns [5].
Unlike other methods used to describe phenology, Four-
ier analysis allows the detection of any periodic structure,
as well as time lags between patterns. Although Fourier
analysis has been widely used to identify periodic patterns
Cecropia phenology at continental scale
P.-C. Zalamea et al.
7
Proc. R. Soc. B
on January 12, 2011 rspb.royalsocietypublishing.org Downloaded from

Page 9

in many fields [11–14], to our knowledge this study rep-
resents the first time that it has been applied to phenology.
We have shown that Fourier analysis can be easily applied
to understand plant phenological patterns and succeeds
where other methods often fail. A future challenge
will be to examine supra-annual patterns, in which the
reproductive pattern is characterized by mast fruiting
on multi-year cycles. It is not possible to detect supra-
annual pattern in data aggregated over a single series of
calendar months; however, if data were aggregated over
an appropriate supra-annual duration, such analyses
may be feasible.
(e) Conclusions
In this study, we found that herbarium collections offer a
powerful tool to determine reproductive phenology at
large geographical scales, and that Fourier spectral analy-
sis is an effective method to characterize phenological
patterns. Application of these tools indicated that Cecropia
phenology is often periodic, in accordance with climate
seasonality, but that time-lags are quite variable and call
forfurtherinvestigationof
Phenomena such as the El Nin ˜o Southern Oscillation
can induce simultaneous anomalies in temperature, pre-
cipitation and irradiance, which in turn can shift
phenological patterns [3]. Thus, large-scale phenological
studies are of central importance to understand how shifts
in climate affect tropical forest dynamics [31]. Our study
is the first to show how herbarium data can convey rich
enough information on phenology to allow detailed and
fruitful ecological analyses at large scales. This suggests
that herbaria can be considered as retrospective observa-
tories to investigate past, present and future plant ecology.
triggering mechanisms.
The authors thank the staff of New York Botanical Garden,
Colombian National Herbarium, Paris Natural History
Museum Herbarium, French Guiana Herbarium, Sinchi
Herbarium,University of
Suriname National Herbarium for help and advice in using
collections. We are grateful to S. Mori, S. Sylva, N. Pe ´rez-
Molie `re,C.Loup,L.-C.
S. Gonzalez, C. Delnatte, M. Correa and M. Werkhoven
for facilitating our work with Cecropia collections. We also
thank J. Dalling, M. Rios, C. Born, A. Jolivot and
O. Taugourdeau for enlightening discussions during data
analyses. The manuscript was improved thanks to valuable
commentsfrom S. Renner,
A. Roddy, N. Brokaw, H. Beeckman and three anonymous
reviewers. This research was partially supported by an
Ecos-Nord Colciencias and Paris 13 University grant
(C08A01),an IRD(Institut
De ´veloppement, France) doctoral grant and a Proyecto
Semilla grant of Los Andes University to P.-C.Z.
PanamaHerbariumand
Jimenez,D. Ca ´rdenas,
D.McKey, J.Dalling,
deRecherche pour le
REFERENCES
1 Leith, H. 1974 Phenology and seasonality modeling. Berlin,
Germany: Springer.
2 Wright, S. J. & Caldero ´n, O. 1995 Phylogenetic patterns
among tropical flowering phenologies. J. Ecol. 83,
937–948. (doi:10.2307/2261176)
3 Wright, S. J. & Caldero ´n, O. 2006 Seasonal, El Nin ˜o and
longer term changes in flower and seed production in a
moist tropical forest. Ecol. Lett. 9, 35–44. (doi:10.1111/
j.1461-0248.2005.00850.x)
4 Borchert, R., Renner, S., Calle, Z., Navarrete, D., Tye,
A., Gautier, L., Spichiger, R. & Von Hildebrand, P.
2005 Photoperiodic induction of synchronous flowering
near the Equator. Nature 433, 627–629. (doi:10.1038/
nature03259)
5 Zimmerman, J. K., Wright, S. J., Caldero ´n, O., Pagan,
M. A. & Paton, S. 2007 Flowering and fruiting phenolo-
gies of seasonal and aseasonal Neotropical forests: the
role of annual changes in irradiance. J. Trop. Ecol. 23,
225–231. (doi:10.1017/S0266467406003890)
6 Tutin, C. E. G. & Fernandez, M. 1993 Relationships
between minimum temperature and fruit production in
some tropical forest trees in Gabon. J. Trop. Ecol. 9,
241–248. (doi:10.1017/S0266467400007239)
7 Borchert, R., Meyer, S. A., Felger, R. S. & Porter-Bolland,
L. 2004 Environmental control of flowering periodicity in
Costa Rican and Mexican tropical dry forests. Global.
Ecol. Biogeogr. 13, 409–425. (doi:10.1111/j.1466-822X.
2004.00111.x)
8 Borchert, R. 1996 Phenology and flowering periodicity of
Neotropical dry forest species: evidence from herbarium
collections. J. Trop. Ecol. 12, 65–80. (doi:10.1017/
S0266467400009317)
9 Boulter, S. L., Kitching, R. L. & Howlett, B. G. 2006
Family, visitors and the weather: patterns of flowering
in tropical rain forests of northern Australia. J. Ecol. 94,
369–382. (doi:10.1111/j.1365-2745.2005.01084.x)
10 Newstrom, L. E., Frankie, G. W. & Baker, H. G. 1994 A
new classification for plant phenology based on flowering
patterns in lowland tropical rain forest trees at La Selva,
Costa Rica. Biotropica 26, 141–159. (doi:10.2307/
2388804)
11 Torrence,C.&Campo,G.P.1998Apracticalguidetowave-
let analysis. Bull. Am. Meteorol. Soc. 79, 61–78. (doi:10.
1175/1520-0477(1998)079,0061:APGTWA.2.0.CO;2)
12 Munoz, F., Cheptou, P. O. & Kjellberg, F. 2007 Spectral
analysis of simulated species distribution maps provides
insights into metapopulation dynamics. Ecol. Model.
205, 314–322. (doi:10.1016/j.ecolmodel.2007.02.020)
13 Keitt, T. H. 2008 Coherent ecological dynamics induced
by large-scale disturbance.
(doi:10.1038/nature06935)
14 Deblauwe, V., Barbier, N., Couteron, P., Lejeune, O. &
Bogaert, J. 2008 The global biogeography of semi-arid
periodic vegetation patterns. Global. Ecol. Biogeogr. 17,
715–723. (doi:10.1111/j.1466-8238.2008.00413.x)
15 Berg, C. C. & Franco, P. 2005 Cecropia. Flora
Neotropica Monograph 94. The Bronx, NY: The
New York Botanical Garden Press.
16 Zalamea, P. C., Stevenson, P. R., Madrin ˜a ´n, S., Aubert,
P. M. & Heuret, P. 2008 Growth pattern and age deter-
minationfor
Cecropia
Am. J. Bot. 95, 263–275. (doi:10.3732/ajb.95.3.263)
17 Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. &
Jarvis,A.2005Veryhighresolutioninterpolatedclimatesur-
faces for global land areas. Int. J. Climatol. 25, 1965–1978.
(doi:10.1002/joc.1276)
18 Olson, D. M. et al. 2001 Terrestrial ecoregions of
the world: a new map of life on earth. Bioscience
51, 933–938. (doi:10.1641/0006-3568(2001)051[0933:
TEOTWA]2.0.CO;2)
19 Bloomfield, P. 2000 Fourier analysis of time series: an intro-
duction. New York, NY: Wiley.
20 Platt, T. & Denman, K. L. 1975 Spectral analysis in ecol-
ogy. Annu. Rev. Ecol. Syst. 6, 189–210. (doi:10.1146/
annurev.es.06.110175.001201)
21 R Development Core Team. 2009 R: a language and
environment for statistical computing. Vienna, Austria: R
Foundation for Statistical Computing. http://www.R-
project.org.
22 Dray, S. & Dufour, A. B. 2007 The ade4 package: imple-
menting the duality diagram for ecologists. J. Stat. Softw.
22, 1–20.
Nature
454, 331–334.
sciadophylla
(Urticaceae).
8 P.-C. Zalamea et al.
Cecropia phenology at continental scale
Proc. R. Soc. B
on January 12, 2011rspb.royalsocietypublishing.org Downloaded from

Page 10

23 Scho ¨ngart, J., Piedade, M. T. F., Ludwigshausen, S.,
Horna, V. & Worbes, M. 2002 Phenology and stem-
growth periodicity of tree species in Amazonian flood-
plain forests. J. Trop. Ecol. 18, 581–597. (doi:10.1017/
S0266467402002389)
24 Swaine, M. D. & Whitmore, T. C. 1988 On the definition
of ecological species groups in tropical rain forests. Plant.
Ecol. 75, 81–86. (doi:10.1007/BF00044629)
25 Bentos, T. V., Mesquita, R. C. G. & Williamson, G. B.
2008Reproductive phenology of
pioneer trees. Trop. Conserv. Sci. 1, 186–203.
26 Guisan, A. & Zimmermann, N. E. 2000 Predictive
habitat distribution models in ecology. Ecol. Model. 135,
147–186. (doi:10.1016/S0304-3800(00)00354-9)
27 Charles-Dominique, P. 1986 Inter-relations between fru-
givorous vertebrates and pioneer plants: Cecropia, birds
and bats in French Guiana. In Frugivores and seed dispersal
(eds A. Estrada & T. H. Fleming), pp. 119–135.
Dordrecht, The Netherlands: Dr. W. Junk Publishers.
Central Amazon
28 Toriola, D. 1998 Fruiting of a 19-year old secondary
forest in French Guiana. J. Trop. Ecol. 14, 373–379.
(doi:10.1017/S0266467498000285)
29 Schulman, L., Toivonen, T. & Ruokolainen, K. 2007
Analysing botanical collecting effort in Amazonia and cor-
recting for it in species range estimation. J. Biogeogr. 34,
1388–1399. (doi:10.1111/j.1365-2699.2007.01716.x)
30 Prather, L. A., Alvarez-Fuentes, O., Mayfield, M. H. &
Ferguson, C. J. 2004 Implications of the decline in
plant collecting for systematic and floristic research.
Syst. Bot. 29, 216–220. (doi:10.1600/0363644047729
74347)
31 Ting, S., Hartley, S. & Burns, K. C. 2008 Global pat-
terns in fruiting seasons. Global. Ecol. Biogeogr. 17,
648–657. (doi:10.1111/j.1466-8238.2008.00408.x)
32 Stevenson, P. R., Castellanos, M. C., Corte ´s, A. I. &
Link, A. 2008 Flowering patterns in a seasonal tropical
lowland forest in western Amazonia. Biotropica 40,
559–567. (doi:10.1111/j.1744-7429.2008.00417.x)
Cecropia phenology at continental scale
P.-C. Zalamea et al.
9
Proc. R. Soc. B
on January 12, 2011rspb.royalsocietypublishing.org Downloaded from